Distress and its influencing factors among Chinese patients with incidental pulmonary nodules: a cross-sectional study

The study aims to investigate the distress level and its influencing factors in Chinese pulmonary nodules patients. A total of 163 outpatients in a tertiary hospital in Xi'an, China, were recruited and investigated by using the Impact of Event Scale, Decision Conflict Scale, Consultation Care Measure, Lung Cancer Worry Scale and a demographic questionnaire. The logistic regression model was used to identify the factors of distress. The mean IES score was 37.35 ± 16.65, which was a moderate level. Patients aged 50–60 years, with higher decision conflicts scores, lower physician–patient communication quality score, and who are anxious about the results of future tests or treatments had higher distress score. Distress levels were moderate in patients with pulmonary nodules. Communication between medical staff and patients is extremely important for the management of pulmonary nodules, which affects the quality of the patient's decision-making and his level of distress.

Lung Cancer has the second-highest incidence rate and the highest mortality rate in the world 1 , and it is the most common cancer in China with new cases and deaths accounting for nearly 40% in the whole world 2 .Early detection is important for lung cancer prevention and management.Results of the National Lung Screening Trial (NLST) showed that screening with low-dose computed tomography (LDCT) can reduce lung cancer mortality by 20% 3 .The latest study shows that one-off LDCT screening in high-risk populations in China can reduce lung cancer mortality by 30% 4 .In 2012, the Chinese government launched a key national plan for public health, Cancer Screening Program in Urban China (CANSPUC), in which participants at high risk aged 40-74 were provided free LDCT test for lung cancer screening 5 .
With the widespread use of computed tomography (CT) technology, pulmonary nodules are becoming more common.Nearly 26.3% of pulmonary nodules were found on annual routine checkups 6 .After being diagnosed, patients have questions about the meaning of the nodules.
With the increasing prevalence of non-smoking related lung cancer in Asian countries, LDCT screening for non-smoking population is widely utilized in Asian countries and regions, such as China, Taiwan (province of China), Korea, Japan.Population anxiety about lung cancer was high in China due to patients died of stage IV lung cancer, unknown risk factors for non-smoking lung cancer, and safe strategies culture in Asian population culture, especially in non-smoking and female populations 7 .
Since pulmonary nodules have the potential to become early lung cancer lesions, patients may become anxious and depressed.Harris et al. believed that this "near cancer" diagnosis would bring various harms to patients, including physical harms, psychological harms, financial strain, and opportunity costs 8 .It is worth noting that very few patients benefit from lung cancer screening (most of them are benign), but nearly all patients are at risk of different types of harms from detection and evaluation of a pulmonary nodule 3,9 .
It is difficult to make an accurate judgment of benign and malignant after the first detection of pulmonary nodules.Patients care about the next step in the diagnosis and treatment plan 10 .Common options for the management of pulmonary nodules in the guidelines include CT surveillance, biopsy, and excision.However, each option has its advantages and disadvantages 11 , and it is a challenge for doctors and patients to choose which one to use.It involves the characteristics of the nodule itself, the patient's history of exposure to lung cancer

Data collection
All the questionnaire and scales were completed by the patient alone.After the participants completed the questionnaire, the researchers immediately checked the questionnaire and collected it on the spot.The data collection timing flow chart see Fig. 1.

Social-demographic characteristics
Socio-demographic questionnaire included age, gender, education level, marital status, employment status, income level, residence, smoking history, relatives with lung cancer, if the patients worried about getting lung cancer someday, and if the patients anxious about the results of future tests/treatments.

Distress
Impact of Event Scale (IES) was used to measure distress.IES, originally designed by Horowitz in 1979, measures an individual's current level of subjective distress due to the impact of a specific event.In 2003, Zhao et al. translated it into a Chinese version 16 .The scale contains 15 items and 2 dimensions, including intrusion (7 items) and avoidance (8 items).Each item was scored on a 4-point scale (0 = not at all, 1 = rarely, 3 = sometimes, and 5 = often).The total scale score ranges from 0 to 75 17 , with higher scores indicating a greater frequency of intrusive thoughts and attempts at avoidance.In this study, according to other research, a total score of 0-25 was classified as mild or below level, and above 26 was considered moderate or high level 18 .

Decision conflict
The Decision Conflict Scale (DCS) was used to measure the decision conflict of patients with pulmonary nodules when deciding the next treatment or surveillance plan.DCS was originally designed by O'Connor in 12 and was later translated into a Chinese version by Li et al. 19 The scale contains 16 items divided into 3 subscales: including information and values, decision support and effectiveness and decision uncertainty.The scale was scored using the Likert 5-level scoring method, and the initial score was converted into 0-100 points to obtain the total score.

Communication quality with doctor
Consultation Care Measure (CCM) is used to measure the quality of communication between doctors and patients about pulmonary nodules.The CCM is designed based on a patient-centered communication model 20,21 to measure patients' perceptions of communication quality after communicating with doctors.The primary measure of the perception of communication was the statement, "The overall quality of communication with your provider (who is caring for your nodule) is excellent, " rated on a 7-point Likert scale from "very strongly www.nature.com/scientificreports/disagree" to "very strongly disagree" strongly agree." 18 .Higher scores indicate that patients perceive the higher quality of communication.

Lung cancer worry
The Lung cancer worry scale (LCWS)was used to measure fear and anxiety in patients with pulmonary nodules about being diagnosed with lung cancer in the future.The scale was modified from the cancer worry scale by changing breast cancer to lung cancer and by changing mammograms to future tests/treatments 22 .Clark et al. applied it for the first time in patients with pulmonary nodules, and there were four questions in the scale.Since we included patients diagnosed for the first time, only two questions were included: "How worried are you about getting lung cancer someday?" and "What is your current anxiety level about the results of future tests/treatments?"These two questions were dichotomized as "not worried" vs. "worried" and "not anxious" vs. "anxious".

Ethics and consent statement
Our research was approved by the Medical Ethics Review Committee of the First Affiliated Hospital of Xian Jiaotong University, and all methods were performed in accordance with the relevant guidelines and regulations.
Patients were informed about the study and invited to participate the survey.The data were anonymous, and coded using participant-created codes.

Data analyses
IBM SPSS Statistics software version 26.0 was used to analyse data.The demographic data were summarized as the means, standard deviations, and ranges for continuous variables and as frequency counts (percentages) for categorical variables.We calculated the means and standard deviations of distress and 2 dimensions, and reported low or mild and moderate or high levels using frequencies and percentages.The differences in distress according to demographic characteristics were analysed using t-tests and one-way analysis of variance (ANOVA).Pearson's correlation analyses were used to investigate the correlations between distress and both decision conflict and communication quality score.Multivariate logistic regression model was constructed to explore the influencing factors of distress among pulmonary nodules patients.All socio-demographic factors, decision conflict, communication quality, lung cancer worry were included in the multilevel analysis.An alpha level of 0.05 was used for the assessment of statistical significance.

Meet inclusion and exclusion criteria
Chest CT test Outpatient doctor confirmed the pulmonary nodules Questionnaire survey   1 shows the relationship between distress and demographic characteristics and lung cancer worry.The correlation analyses showed that decision conflict was positive associated with distress (r = 0.597, p < 0.001) while communication quality was negatively associated with distress (r = 0.403, p < 0.001).

Influencing factors of distress among incidental pulmonary nodules patients
The logistic regression results showed that decision conflict, age, communication quality, and anxiety level about future test results were the main factors that influenced distress among incidental pulmonary nodules patients.

Distress level of pulmonary nodule patients
This study investigated the distress level and its influencing factors in Chinese patients with incidental pulmonary nodules.It was found that the vast majority of patients developed a certain level of distress after being diagnosed with a pulmonary nodule.This result is similar to that of Moseson and Slatore, who used IES to investigate patients with pulmonary nodules 18,24 .Many patients with pulmonary nodules have certain anxiety and distress emotions 25 .Although only about 4% of pulmonary nodules will eventually be diagnosed as lung cancer 3 , it is difficult to make an accurate judgment immediately 26 , so the "near-cancer" diagnosis is a big burden to patients.Some patients even thought they had cancer immediately after being diagnosed with a pulmonary nodule 27 .
Horowitz described the connotations of the 2 dimensions of event impact.Intrusions are thoughts and images that spontaneously, involuntarily appear in the mind, with troubled dreams, strong pangs, and waves of feelings.Avoidance responses include ideational constriction, denial of the meaning and outcome of events, numbness of sensations, inhibition of behavior, or counterphobic activity 28 .This study showed that patients with pulmonary nodules have moderate scores in both dimensions, suggesting that the two types of thoughts exist in patients.When a patient is diagnosed with a pulmonary nodule, there is a spot in the lung, which reminds the patient from time to time that he has a pulmonary nodule and it has the potential to become lung cancer.However, since most pulmonary nodules require regular follow-up, under the advice of doctors, patients will take the initiative to suggest to themselves and try to avoid thinking about it.

Influencing factors of distress
Decision conflict is an important influencing factor of patients' distress.Pulmonary nodules are poorly understood by patients 27 , and their decisions require a wealth of information from their doctors, as well as an understanding of the pros and cons of each option.However, doctors give patients less information due to several factors.This may be related to the fact that pulmonary nodules are very common, doctors need to deal with a large number of patients, and their time and energy are limited 26 .In addition, physicians may be worried that giving too much information would be overwhelming and might actually increase patient distress, so they seldom directly inform the risk of lung cancer and other details about surveillance to their patients 29 .Based on the current context, the British Thoracic Society guidelines suggest that the involvement of lung cancer nurses in further communication with patients would be beneficial 30 .However, these nurses need to be skilled in the prevention and management of lung cancer and pulmonary nodules, such as epidemiology, risk factors, screening methods, and further management of pulmonary nodules (including advantages and disadvantages).In this process, the idea of shared decision-making can be applied.In addition, since in-depth conversation with patients may involve patients in decision-making, nurses need to receive specialized training to provide decision-making Support for patients, such as The Ottawa Decision Support Tutorial 31 .
The communication quality score was also entered into the regression model.It is similar to the results of Slatore et al., the higher the quality of patient self-rated communication, the lower the distress level 24 .In the current clinical decision-making, the paternalistic or informed model is mostly used, which has problems such as low degree of information sharing and low decision satisfaction 23 .A core criterion for high-quality decisionmaking is whether the choice is in line with the patient's values, goals, and preferences.This requires medical staff to learn more about patients' thoughts and consider personal preferences during the communication process.In addition, the communication between doctors and patients about the decision-making of the next diagnosis and treatment plan is not only a one-way information transfer of medical knowledge, but also an emotional exchange.Patients' distress decreases when their clinicians were empathic and generated trust 27,32 .
The regression results showed that age is also a factor affecting distress.Compared with people younger than 50 years old, patients aged 50-60 years have a higher risk of distress.This may be because the age of 50-60 is www.nature.com/scientificreports/still the backbone of the society and the family in the current Chinese society, bearing the heavy burden of the society and the family.When a certain disease is diagnosed, the negative emotions caused by it are heavier.Bivariable analysis by Freiman et al. showed that age over 65 years was a protective factor for distress in patients with pulmonary nodules 33 .Similarly, the results of Li et al. showed that patients with pulmonary nodules between the ages of 40 and 60 had the highest proportion of anxiety, but it was not statistically significant 34 .Further research is needed on the association of age with distress in patients with pulmonary nodules.We found that anxiety about the next test result, but not worry about lung cancer, was an influencing factor of distress.Similar to breast cancer screening, when an individual has a false-positive screening result, it may experience a period of distress.The difference is that distress in false-positive individuals of breast cancer screening is transient, and it disappears immediately after a negative biopsy result 26 .Many patients with pulmonary nodules may be required to follow regular surveillance, leaving them in a state of uncertainty for months or even years.Consequently, the next test results were more closely and directly related to their mood compared with cancer.

Limitations
We should mention that this study has several limitations.Since the design is a cross-sectional study, there may be attentional bias and selection bias in the study.The researchers investigated outpatient patients with pulmonary nodules in a tertiary hospital of a provincial capital city.The level of medical care varies among hospitals of different levels, which may affect the distress among patients with pulmonary nodules.Due to differences www.nature.com/scientificreports/ in the description of pulmonary nodules in imaging reports among different physicians, the characteristics of individual pulmonary nodules were not included in this study.In addition, the quality of doctor-patient communication is measured through patient self-assessment.To truly reflect the quality of communication, it is beneficial to comprehensively consider the evaluation of communication quality by doctors and third parties.Due to the limited sample size, the odds ratio of age group 50-60 might inflated 35 .Finally, Due to the limitations of the cross-sectional study, the causal relationship between the variables needs to be further investigated.

Conclusion
We found that distress levels were moderate in patients with pulmonary nodules.Age, higher decision conflicts scores, lower physician-patient communication quality score, and being anxious about the results of future tests or treatments are influencing factors of distress among pulmonary nodule patients.

Practice implications
In the screening process, in addition to the patients who are finally diagnosed with lung cancer, patients with positive results after screening also need more attention.Due to the heavy clinical tasks of doctors, nurses may play an important role in the health guidance of patients with pulmonary nodules.In this process, patients are informed of the alternative pulmonary nodules management options and the pros and cons of each option.Patient's own decision-making preferences needs more attention, and therapeutic alliance needs to be established between doctor, nurse and patients.This patient-centered communication method can not only effectively eliminate the decision conflicts, but also allow patients to participate in decision-making, which greatly improves the quality of communication and decision.Of course, the feasibility and effectiveness of this model need further experiments to confirm. https://doi.org/10.1038/s41598-023-45708-w